{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,11,2]],"date-time":"2026-11-02T19:54:00Z","timestamp":1793649240593,"version":"4.5.1"},"reference-count":43,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,10,26]],"date-time":"2023-10-26T00:00:00Z","timestamp":1698278400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Neurosci."],"abstract":"<jats:sec><jats:title>Purpose<\/jats:title><jats:p>To classify CVI subtypes and compare the added value of an extensive test battery over a limited test battery in subtype classification of cerebral visual impairment (CVI) in children.<\/jats:p><\/jats:sec><jats:sec><jats:title>Methods<\/jats:title><jats:p>Seventy-five children with a clinical diagnosis of CVI (median [IQR] age: 9 [7\u201312] years) were identified from the medical records. The extensive test battery included visual acuity, contrast sensitivity, ocular alignment, eye movement analysis, visual field analysis, optic nerve head evaluation, and evaluation of visual perception. The limited test battery included visual acuity, contrast sensitivity, ocular alignment, and evaluation of visual perception. Principal component analysis (PCA) followed by cluster analysis was done, for both test batteries separately, to determine the optimum subtype classification for CVI.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>Fifty-one participants with an extensive test battery with mild to moderate visual impairment were included in the main analysis. This resulted in four CVI subtypes for the extensive test battery (subtle characteristics, higher-level visual function deficits, lower-level visual function deficits, and higher- and lower- level visual function deficits) and three CVI subtypes for the limited test battery (subtle characteristics, higher-level visual function deficits, and higher- and lower- level visual function deficits). There were significant differences between the subtypes for 9 out of 10 measures of the extensive and all 4 measures of the limited test battery (<jats:italic>p<\/jats:italic>\u2009&amp;lt;\u20090.05). The subtle characteristics subtype (extensive <jats:italic>n<\/jats:italic>\u2009=\u200919, limited <jats:italic>n<\/jats:italic>\u2009=\u200915) showed near normal lower and higher-level visual functions in both test batteries. The higher-level visual function deficits subtype (extensive <jats:italic>n<\/jats:italic>\u2009=\u200918, limited <jats:italic>n<\/jats:italic>\u2009=\u200924) showed near normal visual acuity combined with significant visual perceptual deficits in both test batteries; accompanied by visual pathways defects and abnormal eye movement behavior in the extensive test battery. The higher- and lower- level visual function deficits subtype (extensive <jats:italic>n<\/jats:italic>\u2009=\u20094, limited <jats:italic>n<\/jats:italic>\u2009=\u200912) showed both higher and lower-level visual function deficits in both test batteries, but application of the extensive test battery revealed additional visual pathways defects and abnormal eye movement behavior. The lower-level visual function deficits CVI subtype (extensive <jats:italic>n<\/jats:italic>\u2009=\u200910) was a new subtype identified by the extensive test battery. This subtype showed lower-level visual function deficits together with abnormal eye movement measures.<\/jats:p><\/jats:sec><jats:sec><jats:title>Conclusion<\/jats:title><jats:p>This data-driven study has provided meaningful CVI subtype classifications based on the outcomes of various key functional and structural measures in CVI diagnosis. Comparison of the extensive test battery to the limited test battery revealed the added value of an extensive test battery in classifying CVI. The outcomes of this study, therefore, have provided a new direction in the area of CVI classification.<\/jats:p><\/jats:sec>","DOI":"10.3389\/fnins.2023.1266201","type":"journal-article","created":{"date-parts":[[2023,10,26]],"date-time":"2023-10-26T13:20:07Z","timestamp":1698326407000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":7,"title":["Childhood cerebral visual impairment subtype classification based on an extensive versus a limited test battery"],"prefix":"10.3389","volume":"17","author":[{"given":"Jannet","family":"Philip","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bianca","family":"Huurneman","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nomdo M.","family":"Jansonius","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Antonius H. N.","family":"Cillessen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Frouke N.","family":"Boonstra","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2023,10,26]]},"reference":[{"key":"ref1","first-page":"101","article-title":"Groningen edge contrast chart (GECKO) and glare measurements","volume-title":"Low vision. Amsterdam","author":"Aart Kooijman","year":"1994"},{"key":"ref2","doi-asserted-by":"publisher","first-page":"555","DOI":"10.1016\/0042-6989(94)90168-6","article-title":"The Cardiff acuity test used for measuring visual acuity development in toddlers","volume":"34","author":"Adoh","year":"1994","journal-title":"Vis. Res."},{"key":"ref3","doi-asserted-by":"publisher","first-page":"386","DOI":"10.3390\/genes13020386","article-title":"Cluster-based analysis of retinitis Pigmentosa modifiers using Drosophila eye size and gene expression data","volume":"13","author":"Amstutz","year":"2022","journal-title":"Genes."},{"key":"ref4","doi-asserted-by":"publisher","first-page":"104391","DOI":"10.1016\/j.ridd.2022.104391","article-title":"Including visual orienting functions into cerebral visual impairment screening: reliability, variability, and ecological validity","volume":"132","author":"Ben Itzhak","year":"2023","journal-title":"Res. Dev. Disabil."},{"key":"ref5","doi-asserted-by":"publisher","first-page":"189","DOI":"10.3109\/01658107.2014.902971","article-title":"Peripheral visual fields in children and young adults using semi-automated kinetic perimetry: feasibility of testing, normative data, and repeatability","volume":"38","author":"Bjerre","year":"2014","journal-title":"Neuro-Ophthalmology"},{"key":"ref6","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fnhum.2022.727565","article-title":"The multidisciplinary guidelines for diagnosis and referral in cerebral visual impairment","volume":"16","author":"Boonstra","year":"2022","journal-title":"Front. Hum. Neurosci."},{"key":"ref7","doi-asserted-by":"publisher","first-page":"1149","DOI":"10.1016\/j.ridd.2010.08.001","article-title":"Cerebral visual impairment: which perceptive visual dysfunctions can be expected in children with brain damage? A systematic review","volume":"31","author":"Boot","year":"2010","journal-title":"Res. Dev. Disabil."},{"key":"ref8","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/1471-2415-14-59\/TABLES\/4","article-title":"Low vision due to cerebral visual impairment: differentiating between acquired and genetic causes","volume":"14","author":"Bosch","year":"2014","journal-title":"BMC Ophthalmol."},{"key":"ref9","doi-asserted-by":"publisher","first-page":"272","DOI":"10.3109\/07380577.2015.1136757","article-title":"Validity and reliability of the developmental test of visual perception","volume":"30","author":"Brown","year":"2016","journal-title":"Occup Ther Health Care"},{"key":"ref10","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fnhum.2021.711873","article-title":"Higher visual function deficits in children with cerebral visual impairment and good visual acuity","volume":"15","author":"Chandna","year":"2021","journal-title":"Front. Hum. Neurosci."},{"key":"ref11","doi-asserted-by":"publisher","first-page":"2743","DOI":"10.1016\/S0042-6989(97)00437-9","article-title":"Visual field extent in children 3.5-30 months of age tested with a double-arc LED perimeter","volume":"38","author":"Dobson","year":"1998","journal-title":"Vis. Res."},{"key":"ref12","doi-asserted-by":"publisher","first-page":"69","DOI":"10.1007\/s10633-013-9382-1","article-title":"The spectrum of cerebral visual impairment as a sequel to premature birth: an overview","volume":"127","author":"Dutton","year":"2013","journal-title":"Doc. Ophthalmol."},{"key":"ref13","doi-asserted-by":"publisher","first-page":"294","DOI":"10.1177\/08830738070220030801","article-title":"Spectrum of visual disorders in children with cerebral visual impairment","volume":"22","author":"Fazzi","year":"2007","journal-title":"J. Child Neurol."},{"key":"ref14","doi-asserted-by":"publisher","first-page":"e1010","DOI":"10.1111\/aos.13755","article-title":"Correlation of morphological parameters and visual acuity with neurological development in former preterm children aged 4\u201310 years","volume":"96","author":"Fie\u00df","year":"2018","journal-title":"Acta Ophthalmol."},{"key":"ref15","doi-asserted-by":"publisher","first-page":"49","DOI":"10.3389\/fnint.2015.00049","article-title":"Motion perception: a review of developmental changes and the role of early visual experience","volume":"9","author":"Hadad","year":"2015","journal-title":"Front. Integr. Neurosci."},{"key":"ref16","doi-asserted-by":"publisher","first-page":"100","DOI":"10.2307\/2346830","article-title":"Algorithm AS 136: a k-means clustering algorithm","volume":"28","author":"Hartigan","year":"1979","journal-title":"J R Statistic. Soc."},{"key":"ref17","doi-asserted-by":"publisher","first-page":"369","DOI":"10.1038\/SJ.EYE.6700364","article-title":"Visual function in the brain-damaged child","volume":"17","author":"Hoyt","year":"2003","journal-title":"Eye (Lond.)"},{"key":"ref9001","doi-asserted-by":"publisher","DOI":"10.1002\/14651858.CD011221.pub2","article-title":"Tests for detecting strabismus in children aged 1 to 6 years in the community","volume":"11","author":"Hull","year":"2017","journal-title":"Cochrane Database of Systematic Reviews"},{"key":"ref18","doi-asserted-by":"publisher","first-page":"363","DOI":"10.1080\/01658107.2019.1583760","article-title":"Ganglion cell topography indicates pre- or postnatal damage to the retro-geniculate visual system, predicts visual field function and may identify cerebral visual impairment in children \u2013 a multiple case study","volume":"43","author":"Jacobson","year":"2019","journal-title":"Neuro-Ophthalmology"},{"key":"ref19","doi-asserted-by":"publisher","first-page":"1100","DOI":"10.1111\/DMCN.14545","article-title":"Retinal ganglion cell topography predicts visual field function in spastic cerebral palsy","volume":"62","author":"Jacobson","year":"2020","journal-title":"Dev. Med. Child Neurol."},{"key":"ref20","doi-asserted-by":"publisher","first-page":"104094","DOI":"10.1016\/j.bspc.2022.104094","article-title":"Prediction of dyslexia severity levels from fixation and saccadic eye movement using machine learning","volume":"79","author":"JothiPrabha","year":"2023","journal-title":"Biomed Signal Process Control"},{"key":"ref21","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1167\/iovs.62.6.15","article-title":"Cerebral visual impairment characterized by abnormal visual orienting behavior with preserved visual cortical activation","volume":"62","author":"Kelly","year":"2021","journal-title":"Invest. Ophthalmol. Vis. Sci."},{"key":"ref22","doi-asserted-by":"publisher","first-page":"1393","DOI":"10.1016\/j.ridd.2014.03.038","article-title":"Viewing behavior and related clinical characteristics in a population of children with visual impairments in the Netherlands","volume":"35","author":"Kooiker","year":"2014","journal-title":"Res. Dev. Disabil."},{"key":"ref23","doi-asserted-by":"publisher","first-page":"690","DOI":"10.1177\/0883073814539556","article-title":"The relationship between visual orienting responses and clinical characteristics in children attending special education for the visually impaired","volume":"30","author":"Kooiker","year":"2015","journal-title":"J. Child Neurol."},{"key":"ref24","doi-asserted-by":"publisher","first-page":"599","DOI":"10.1111\/AOS.13038","article-title":"Quantification of visual function assessment using remote eye tracking in children: validity and applicability","volume":"94","author":"Kooiker","year":"2016","journal-title":"Acta Ophthalmol."},{"key":"ref25","first-page":"249","article-title":"Brain visual impairment in childhood: Mini review","volume":"14","author":"Kozeis","year":"2010","journal-title":"Hippokratia"},{"key":"ref26","doi-asserted-by":"publisher","first-page":"245","DOI":"10.1097\/00006324-200404000-00010","article-title":"Clinical testing of contrast sensitivity in children: age-related norms and validity","volume":"81","author":"Leat","year":"2004","journal-title":"Optom. Vis. Sci."},{"key":"ref27","doi-asserted-by":"publisher","first-page":"5","DOI":"10.1016\/j.spen.2019.05.003","article-title":"Profiling children with cerebral visual impairment using multiple methods of assessment to aid in differential diagnosis","volume":"31","author":"Lueck","year":"2019","journal-title":"Semin. Pediatr. Neurol."},{"key":"ref28","doi-asserted-by":"publisher","first-page":"89","DOI":"10.1007\/s10633-013-9405-y","article-title":"Cerebral visual dysfunction in prematurely born children attending mainstream school","volume":"127","author":"Macintyre-B\u00e9on","year":"2013","journal-title":"Doc. Ophthalmol."},{"key":"ref29","doi-asserted-by":"publisher","first-page":"619","DOI":"10.1016\/S0042-6989(97)88335-6","article-title":"Long-term reliability and predictive validity of the teller acuity card procedure","volume":"38","author":"Mash","year":"1998","journal-title":"Vis. Res."},{"key":"ref30","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1016\/j.spen.2019.05.004","article-title":"Cerebral visual impairment and clinical assessment: the European perspective","volume":"31","author":"Ortibus","year":"2019","journal-title":"Semin. Pediatr. Neurol."},{"key":"ref31","doi-asserted-by":"publisher","first-page":"196","DOI":"10.1111\/cxo.12155","article-title":"Identifying and characterising cerebral visual impairment in children: a review","volume":"97","author":"Philip","year":"2014","journal-title":"Clin. Exp. Optom."},{"key":"ref32","doi-asserted-by":"publisher","first-page":"489","DOI":"10.1136\/bjo.86.5.489","article-title":"Use of Lea symbols in young children","volume":"86","author":"Repka","year":"2002","journal-title":"Br. J. Ophthalmol."},{"key":"ref33","doi-asserted-by":"publisher","first-page":"484","DOI":"10.1167\/IOVS.05-0529","article-title":"Changes in the optic disc excavation of children affected by cerebral visual impairment: a tomographic analysis","volume":"47","author":"Ruberto","year":"2006","journal-title":"Invest. Ophthalmol. Vis. Sci."},{"key":"ref34","doi-asserted-by":"publisher","first-page":"303","DOI":"10.1111\/DMCN.14710","article-title":"Visual function subtyping in children with early-onset cerebral visual impairment","volume":"63","author":"Sakki","year":"2021","journal-title":"Dev. Med. Child Neurol."},{"key":"ref35","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fnhum.2021.765371","article-title":"Exploratory investigation of brain MRI lesions according to whole sample and visual function subtyping in children with cerebral visual impairment","volume":"15","author":"Sakki","year":"2022","journal-title":"Front. Hum. Neurosci."},{"key":"ref36","doi-asserted-by":"publisher","first-page":"424","DOI":"10.1136\/bjophthalmol-2017-310694","article-title":"Is there consensus in defining childhood cerebral visual impairment? A systematic review of terminology and definitions","volume":"102","author":"Sakki","year":"2018","journal-title":"Br. J. Ophthalmol."},{"key":"ref37","doi-asserted-by":"publisher","first-page":"2885","DOI":"10.1167\/iovs.09-4670","article-title":"Profile of refractive errors in cerebral palsy: impact of severity of motor impairment (GMFCS) and CP subtype on refractive outcome","volume":"51","author":"Saunders","year":"2010","journal-title":"Investig. Ophthalmol. Vis. Sci."},{"key":"ref38","doi-asserted-by":"publisher","first-page":"239","DOI":"10.1007\/BF00417545","article-title":"Automatic (Octopus) and manual (Goldmann) perimetry in glaucoma","volume":"213","author":"Schmied","year":"1980","journal-title":"Albrecht Von Graefes Arch. Klin Exp. Ophthalmol."},{"key":"ref39","doi-asserted-by":"publisher","first-page":"593","DOI":"10.1038\/eye.2011.333","article-title":"Validation of printed and computerised crowded kay picture logMAR tests against gold standard ETDRS acuity test chart measurements in adult and amblyopic paediatric subjects","volume":"26","author":"Shah","year":"2012","journal-title":"Eye"},{"key":"ref41","doi-asserted-by":"publisher","first-page":"102430","DOI":"10.1016\/j.nicl.2020.102430","article-title":"Structural brain damage and visual disorders in children with cerebral palsy due to periventricular leukomalacia","volume":"28","author":"Tinelli","year":"2020","journal-title":"NeuroImage"},{"key":"ref42","doi-asserted-by":"publisher","first-page":"78","DOI":"10.3109\/09273972.2012.680232","article-title":"Diagnosing cerebral visual impairment in children with good visual acuity","volume":"20","author":"van Genderen","year":"2012","journal-title":"Strabismus"},{"key":"ref43","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fnhum.2021.673342","article-title":"Behavioural features of cerebral visual impairment are common in children with down syndrome","volume":"15","author":"Wilton","year":"2021","journal-title":"Front. Hum. Neurosci."}],"updated-by":[{"DOI":"10.3389\/fnins.2024.1462687","type":"corrigendum","label":"Corrigendum","source":"publisher","updated":{"date-parts":[[2024,8,20]],"date-time":"2024-08-20T00:00:00Z","timestamp":1724112000000}}],"container-title":["Frontiers in Neuroscience"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fnins.2023.1266201\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,8,20]],"date-time":"2024-08-20T09:10:40Z","timestamp":1724145040000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fnins.2023.1266201\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,10,26]]},"references-count":43,"alternative-id":["10.3389\/fnins.2023.1266201"],"URL":"https:\/\/doi.org\/10.3389\/fnins.2023.1266201","relation":{"corrigendum":[{"id-type":"doi","id":"10.3389\/fnins.2024.1462687","asserted-by":"object"}]},"ISSN":["1662-453X"],"issn-type":[{"value":"1662-453X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,10,26]]},"article-number":"1266201"}}